In his theory of evolution, Darwin recognized that the conditions of life play a role in the generation of hereditary variations, as well as in their selection. However, as evolutionary theory was developed further, heredity became identified with genetics, and variation was seen in terms of combinations of randomly generated gene mutations. We argue that this view is now changing, because it is clear that a notion of hereditary variation that is based solely on randomly varying genes that are unaffected by developmental conditions is an inadequate basis for evolutionary theories. Such a view not only fails to provide satisfying explanations of many evolutionary phenomena, it also makes assumptions that are not consistent with the data that are emerging from disciplines ranging from molecular biology to cultural studies. These data show that the genome is far more responsive to the environment than previously thought, and that not all transmissible variation is underlain by genetic differences. In Evolution in Four Dimensions (2005) we identify four types of inheritance (genetic, epigenetic, behavioral, and symbol-based), each of which can provide variations on which natural selection will act. Some of these variations arise in response to developmental conditions, so there are Lamarckian aspects to evolution. We argue that a better insight into evolutionary processes will result from recognizing that transmitted variations that are not based on DNA differences have played a role. This is particularly true for understanding the evolution of human behavior, where all four dimensions of heredity have been important.

Jablonka & Lamb (J&L) reject “the dreaded memes,” but memetics can explain human uniqueness and culture (as a product of the ability to imitate) without depending on their slippery notion of symbolism. Modern memes show the beginnings of a division into replicators and vehicles, and the replacement of reconstructive processes with systems of blind copying, variation, and selection.

This book presents a survey of the molecular basis for the genetic control of living organisms and their evolution. The authors consider four dimensions of control over what shapes life forms: genetic, epigenetic, behavioral, and symbolic/cultural. They pay particular attention to the epigenetic realm, and they defend a view recognizing the genetic incorporation of acquired characteristics – a neo-Lamarckian tack.

Environment can provide information used in development – information that can appear to be genetically given and that was previously assumed to be so. Examples include growth of the eye until it achieves good focus, and structuring of receptive fields in the visual cortex by environmental information. The process can be called one-generation Lamarckism because information acquired from the environment is used to structure the organism and because the capacity to acquire this information is inherited.

Jablonka & Lamb (J&L) have presented a number of different possible mechanisms for finessing design. The extra-genetic nature of these mechanisms has led them to challenge orthodox neo-Darwinian views. However, these mechanisms are for calibration and have been designed by natural selection. As such, they add detail to our knowledge, but neo-Darwinism is sufficiently resourced to account for them.

Evolution in Four Dimensions claims that epigenetic, behavioral, and symbolic inheritance systems should be considered equal partners to genetics in evolutionary biology. The evidence for, and applicable scope of, these additional inheritance systems is limited, particularly with regard to areas involving learning. It is unclear how including these extra dimensions in mainstream evolutionary thinking translates into testable hypotheses for a productive research program.

Although the first three dimensions of evolution outlined by Jablonka & Lamb (J&L) are persuasively presented as aspects of evolutionary science, the fourth dimension, symbolic evolution, is problematic: Though it may in some metaphorical sense be happening, there cannot be a science of symbolic evolution. Symbolic evolution essentially involves meaning, which, besides being nonphysical, resolutely resists scientific categorization.

The argument that heritable epigenetic change plays a distinct role in evolution would be strengthened through recognition that it is what bootstrapped the origin and early evolution of life, and that, like behavioral and symbolic change, it is non-Darwinian. The mathematics of natural selection, a population-level process, is limited to replication with negligible individual-level change that uses a self-assembly code.

Understanding evolution beyond a gene-centered vision is a fertile ground for new questions and approaches. However, in this systemic perspective, we take issue with the necessity of the concept of information. Through the example of brain and language evolution, we propose the autonomous systems theory as a more biologically relevant framework for the evolutionary perspective offered by Jablonka & Lamb (J&L).

Evolution in Four Dimensions argues convincingly that non-genetic inheritance systems have the potential to be agents of evolution and that, in some circumstances, acquired information can be heritable. However, we found the authors' four-dimensional approach to evolution problematic, and doubt that symbolic evolution can be adequately modeled as a distinct dimension of organismal evolution.

Jablonka & Lamb's (J&L's) extended evolutionary theory is more amenable to being applied to human cultural change than standard neo-Darwinian evolutionary theory. However, the authors are too quick to dismiss past evolutionary approaches to human culture. They also overlook a potential parallel between evolved genetic mechanisms that enhance evolvability and learned cognitive mechanisms that enhance learnability.

Jablonka & Lamb (J&L) refer only implicitly to aspects of cognitive competence that preceded both evolution of human language and language learning in children. These aspects are important for evolution and development but need to be understood using the design-stance, which the book adopts only for molecular and genetic processes, not for behavioural and symbolic processes. Design-based analyses reveal more routes from genome to behaviour than J&L seem to have considered. This both points to gaps in our understanding of evolution and epigenetic processes and may lead to possible ways of filling the gaps.

Jablonka & Lamb's (J&L's) book is refreshing in that it debunks the exclusively gene-centered approach used these days to explain almost anything about life and human behavior. The book is very accessible and most convincing when the authors discuss biological theories of genetic and epigenetic inheritance, but it does not shy away from the more slippery terrain of behavioral and symbolic inheritance, and specifically the origins of language. But is the analogy appropriate?

A strength of Jablonka & Lamb's (J&L's) book lies in its accessible as well as thorough treatment of genetic and epigenetic inheritance. The authors also provide a stimulating framework integrating evolutionary research across disciplines. A weakness is its unsystematic treatment of the interaction between behavioral and symbolic inheritance, particularly in their discussion of language.

The commentaries on Evolution in Four Dimensions reflect views ranging from total adherence to gene-centered neo-Darwinism, to the acceptance of non-genetic and Lamarckian processes in evolution. We maintain that genetic, epigenetic, behavioral, and cultural variations have all been significant, and that the developmental aspects of heredity and evolution are an important bridge that can unite seemingly conflicting research programs and different disciplines.

Innovation is a key component of most definitions of culture and intelligence. Additionally, innovations may affect a species' ecology and evolution. Nonetheless, conceptual and empirical work on innovation has only recently begun. In particular, largely because the existing operational definition (first occurrence in a population) requires long-term studies of populations, there has been no systematic study of innovation in wild animals. To facilitate such study, we have produced a new definition of innovation: Innovation is the process that generates in an individual a novel learned behavior that is not simply a consequence of social learning or environmental induction. Using this definition, we propose a new operational approach for distinguishing innovations in the field. The operational criteria employ information from the following sources: (1) the behavior's geographic and local prevalence and individual frequency; (2) properties of the behavior, such as the social role of the behavior, the context in which the behavior is exhibited, and its similarity to other behaviors; (3) changes in the occurrence of the behavior over time; and (4) knowledge of spontaneous or experimentally induced behavior in captivity. These criteria do not require long-term studies at a single site, but information from multiple populations of a species will generally be needed. These criteria are systematized into a dichotomous key that can be used to assess whether a behavior observed in the field is likely to be an innovation.

Captive or experimental studies may be of greater utility than field studies in documenting novel behaviors. Social hierarchy affects the spread of innovations. Innovative species should also be found in cases where sociality is low or absent.

Indirect identification of innovations in wild populations involves inferring past, unobserved behavioral events. Such historical inference can make simple use of present distribution patterns of differently behaving individuals, but population genetic studies are a potential source of complementary relevant information. Methodological lessons can be taken from phylogeography, that is, molecular approaches to the history of population spatial distribution patterns and gene flows. Opportunities for such studies in primates should increase with the developing population genetic studies used for management and conservation purposes.

Ramsey et al.'s article provides a more sensitive framework for comparative innovation than others' operationalisations have done. Nevertheless, a methodology has to be elaborated in order to determine to what degree a behaviour is novel. Psychological processes have to be considered when evaluating the value of reference groups and in order to figure out where to look for innovation.

Ramsey et al. present an ingenious method to study behavioral novelty under field conditions within relatively narrow time constraints. This evokes discussion of lateral spread of innovation from individual to individual versus vertical spread from generation to generation. This discussion of incipient culture helps to place the traditional biological tool of cross-fostering into philosophical and anthropological context.